Rapid stress response in post-nesting Kemp's ridley turtle
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
SALAMANDRA 57(1): 146–150
Ozzy S. Vásquez Bultrón et al.
SALAMANDRA
15 February 2021 ISSN 0036–3375 German Journal of Herpetology
Rapid stress response in post-nesting Kemp’s ridley turtle
(Lepidochelys kempii)
Ozzy S. Vásquez-Bultrón1, Diana E. Moreno-Espinoza1,
Laura T. Hernández-Salazar1 & Jorge E. Morales-Mávil1
1)
Laboratorio Biología de la Conducta, Instituto de Neuroetología, Universidad Veracruzana, Avenida Dr. Luis Castelazo Ayala s/n,
Colonia Industrial Ánimas, C.P. 91190, Xalapa, Veracruz, México
Corresponding author: Jorge E. Morales-Mávil, e-mail: jormorales@uv.mx
Manuscript received: 1 October 2020
Accepted: 7 January 2021 by Stefan Lötters
Abstract. Vertebrate’s stress response plays a significant role in helping individuals adapt to changing environments. One
of the most challenging stages in female turtles’ life cycle is during oviposition, especially when the turtles’ nest during the
daytime and have to face massive nesting events (arribadas), limited space on the beach, and high temperatures. The Kemp’s
ridley sea turtle (Lepidochelys kempii) is the smallest sea turtle, which has to withstand high temperatures during the nesting
process due to its diurnal habits. Our objective was to determine corticosterone concentration as a response to induced stress
and estimate its variations at the beginning, middle, and end of the nesting season. We measured the corticosterone concen-
tration in serial blood samples (0, 20, 40, and 60 min.) in 22 Kemp’s ridley sea turtles during the beginning, the middle, and
the end of the nesting season. Our results show that the turtles had a significant increase in corticosterone levels at 20 min. af-
ter the onset of stress, and we found that corticosterone decreased at the end of the nesting season. The results point to a rapid
response of the hypothalamic–pituitary-adrenal axis. We suggest that glucocorticoid levels return to baseline at the end of the
breeding season, and modulation may allow successful completion of nesting throughout the entire seasonal nesting period.
Key words. Testudines, Cheloniidae, Carettinae, Corticosterone, Gulf of Mexico, nesting, sea turtles, stress protocol.
Introduction
Rostal et al. 2001, Al-Habsi et al. 2006; Chelonia mydas
During the sea turtle nesting period, nesting females face and Eretmochelys imbricata: Jessop 2001).
several environmental factors that may cause stress and in- However, it is not clear whether this modulation of the
crease their glucocorticoid levels; for example, the fluctua- HPA axis develops in the same way in all species of sea
tion of water temperature (Hunt et al. 2012) and the pro- turtles. The Kemp’s ridley sea turtle, Lepidochelys kem-
longed period of aphagia (Cherel et al. 1988, Williams pii (Garman, 1880), is the smallest sea turtle and due to
et al. 2008) documented in the green sea turtle, Chelonia its diurnal habits must withstand higher environmental
mydas (Linnaeus, 1758) (Hays et al. 2002) and in the temperatures during the nesting process than other spe-
hawksbill turtle, Eretmochelys imbricata (Linnaeus, 1766) cies, which exhibit nocturnal nesting. This study aims to
(Santos et al. 2010) are frequents stressors. Sustained estimate corticosterone concentration in L. kempii as a re-
aphagia harms the females’ body condition, deteriorat- sponse to induced stress and determine its variations at the
ing their physical condition and body mass (Cherel et al. beginning, middle, and end of the nesting season.
1988). However, green sea turtles seem to tolerate periods of
aphagia, demonstrating decreased corticosterone levels at Materials and methods
the end of the reproductive season, suggesting that their nu-
tritional status is not compromised (Hamann et al. 2002). The study was conducted on Santander beach, Alto Lu-
The reproduction of marine chelonians depends on sev- cero municipality, Veracruz, Mexico (19°5’27.80’’ N,
eral factors, such as the fluctuation of corticosterone dur- 96°31’34.49’’ W and 19°51’38.58’’ N, 96°27’46.47’’ W). We
ing the nesting season (Valverde et al. 1999, Stephenson collected the Kemp’s ridley plasma samples between April
et al. 2000). Nesting female sea turtles require hypotha- and June 2017 and during the same period in 2018. Plas-
lamic–pituitary-adrenal (HPA) modulation to assist with ma samples were collected from 22 turtles. Mean (± SD)
sufficient energy to perform and complete oviposition suc- of straight carapace length was 640.03 ± 20.22 mm (range:
cessfully (Lepidochelys olivacea (Eschscholtz, 1829): Val- 700.87–590.69 mm), and the mean mass was 3500.18 ±
verde et al. 1999; Dermochelys coriacea (Vandelli, 1761): 300.89 g (range: 4400.39–2700.34 g).
© 2021 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany
146 access at http://www.salamandra-journal.com
OpenRapid stress response in post-nesting Lepidochelys kempii
Stress protocol and sample collection Data analysis
We carried out daytime surveys on the beach between 06:00 We determined normality using Shapiro-Wilk tests. We
and 18:00 h. When we found a nesting female, we waited performed a repeated measures Friedman test to deter-
for oviposition to end and upon its completion immediately mine whether non-zero CORT concentration ratio times
collected the first blood sample (0 min.). We then performed differed, and applied Dunn’s post hoc tests. We used ANO-
the stress protocol by laying the female on her shell for an VA or Kruskal-Wallis to determine whether the beginning,
hour and we collected 10 mm blood samples after 20 min., the middle, and the end of the nesting season differed sta-
40 min., and 60 min. (modified from Valverde et al. 1999). tistically. All statistical analyses were performed in R ver-
We collected blood samples by puncturing the cervical sinus sion 3.6.2 (R Core Team 2013).
using 21 g x 32 mm needles (Owens & Ruiz 1980), after dis-
infection with iodine. Blood samples (10 ml) were placed in
heparin tubes inside a cooler with cooling gels. In the labo- Results
ratory, the plasma was centrifuged (3,000 rpm) for 10 min.
The plasma was stored in Eppendorf tubes at -20°C (Val- We recorded significant differences between the CORT
verde et al. 1999). We followed the Guidelines for Use of concentrations from the 22 samples taken at different times
Live Amphibians and Reptiles in Field and Laboratory Re- (Friedman, F = 30.6; df = 3; p < 0.001). The mean concen-
search (American Society of Ichthyologists and Herpetolo- tration of corticosterone at: T-0 was 6.02 ± 3.21 ng/mL, T-20
gists 2004) were followed for the management of all animals was 8.20 ± 3.36 ng/mL, T-40 was 9.74 ± 4.26 ng/mL and
used in the study. In addition, we adhered to the indica- T-60 was 12.22 ± 4.57 ng/mL (Fig. 1). The post hoc results
tions of the Mexican regulations for sea turtles, NOM-162- showed significant differences in the increase in CORT in
SEMARNAT-2012, and complied with protocols approved all treatments with respect to time zero, after 20 min. (p =
by the Secretariat of the Environment and Natural Resourc- 0.0345), 40 min. (p < 0.0034) and 60 min. (p < 0.001). The
es of the Mexican Government (SGPA/DGVS/05014/17 highest CORT concentration was at T-60 (p < 0.01).
and SGPA/DGVS/002776/18). We divided the nesting sea- The CORT concentration differed significantly between
son into three periods: beginning (1–27 April), middle (28 the beginning, middle and end of the nesting season (χ² =
April–25 May), and end (26 May–22 June). 7.05, gl = 3, p = 0.07). A significant increase in T-60 (p =
0.031) compared T-0 was observed (Fig. 2a). T-0 and T-60
differed significantly during the middle season (χ² = 13.8,
Analysis of corticosterone (CORT) concentration df = 3, p = 0.00319), with a significant increase at 60 min.
(p = 0.0275) (Fig. 2b). At the end of the season, differenc-
We analyzed plasma CORT concentration in the laborato- es were found between the times of the samples in CORT
ries of the Faculty of Medicine and the Brain Research Cent- concentration (χ² = 17.914, df = 3, value of p = 0.0004581),
er of the Universidad Veracruzana using the Corticosterone with a significant increase occurring after 20 min. of test-
(Human, Rat, Mouse) ELISA kit from IBL International. ing (p = 0.0456) (Fig. 2c).
All samples were duplicated (100 μl of solution per sam- We found a significant decrease in CORT concentrations
ple) in polystyrene plates with flat bottom wells. Accord- at the end of the nesting season (F = 5.6126; df = 2, p-value
ingly, plasma samples and controls were conjugated with = 0.01423), with differences between the beginning and the
200 μL of horseradish peroxidase signal amplifier and then end of the nesting season (p = 0.0206571), and the middle
mixed for 10 sec., and we incubated at room temperature
for one hour. The plates were washed three times with di-
luted washing solution (400 μl per well). We added 100 μL
of substrate solution (Tetramethylbenzidine: TMB) to each
well. We incubated the mixture for 15 min. at room tem-
perature and stopped the enzymatic reaction by adding 50
μL of stop solution to each well. We read the solution using
the microtiter plate reader 10 min. after adding the stop so-
lution. We calibrated the curve with the Myassays program
by using four logistic parameters (4PL), as indicated in the
kit. Analytical validation was obtained using ANOVA with
parallelism to the standard curve with two samples in se-
rial dilution. The curves were parallel to the standard curve
(P > 0.05). We obtained an intra-assay coefficient of vari-
ation ranging from 6 to 12.8 % (n = 2), with the repetition
of one sample in the same assay. The coefficient of varia-
tion between trials ranged from 11 to 20% (n = 2) measuring Figure 1. Variation of corticosterone concentration according to
the same sample and different trials. Analytical validations sample times of stress protocol in Lepidochelys kempii nesting
demonstrated the accuracy and precision of the assays. season. Different letters indicate significant differences.
147Ozzy S. Vásquez Bultrón et al.
and the end of the nesting season (p = 0.0327). We did not stimuli reached one hour. The rapid response we found in
find differences in CORT concentrations between the 60- L. kempii is faster than the response reported for L. oliva-
min. records at the beginning, middle, and end of the nest- cea during a similar stress protocol, where the response oc-
ing season (χ² = 1.1098, df = 2, p-value = 0.5741) (Fig. 3). curred 120 min. after the stressor was applied (Valverde
et al. 1999). The results are in line with our hypothesis; the
Kemp’s ridley sea turtle modulates stress response differ-
Discussion ently to other sea turtles species when faced with a stressful
stimulus, considering that Kemp’s ridley sea turtle, is the
The stress protocol shows that Kemp’s ridley sea turtles smallest sea turtle and has diurnal habits that force them
can increase corticosterone concentration within 20 min. withstand higher environmental temperatures during the
in response to stress. This response was similar at the be- nesting unlike other species which exhibit nocturnal nest-
ginning, middle, and end of the nesting season and cor- ing. We therefore, found differences in the stress response
ticosterone levels were highest when exposure to intense time between a diurnal nesting species and a nocturnal
nesting species of sea turtle.
The increases in CORT concentration in response to
stress are similar to those found in immature L. kempii in-
dividuals during capture (Gregory & Schmid 2001). Im-
mature individuals showed a low response to stress at 13 h
of transported (7.05 ± 2.82 ng/ml), while individuals trans-
ported at 26 h had a mean increase in corticosterone of
11.56 ± 3.42 ng/ml (Hunt et al. 2016). The corticosterone
concentration reported by Hunt et al. (2016) is similar to
the concentrations we report (12.61 ± 3.39 ng/ml). Our data
suggests that in adult females Kemp’s ridley, the response
time and glucocorticoid concentration are similar to im-
mature individuals when they face stressors factors differ-
Time (min), onset of season ent.
The high concentration of glucocorticoids suggests that
nesting Kemp’s ridley sea turtles have a different and fast-
er response capacity than olive ridley turtles to stressors.
Different stressors occur during daytime nesting than at
nighttime nesting and could be affecting the increase in
CORT concentration, such as sun exposure and overheat-
ing of the sand (Spotila & Standora 1985), as well as a
more significant human presence and increased number of
predators (Wingfield et al. 1998). In addition, L. kempii
is the smallest marine turtle (Márquez 1996, Pritchard
& Mortimer 2000), and therefore has a lower resistance
Time (min), middle of season
Onset Middle End
Time (min), end of season Season
Figure 2. Differences between sample times in Kemp’s sea rid- Figure 3. Differences in corticosterone concentration in T-0 dur-
ley turtles nesting season: A) onset, p = 0.0311; B) middle, p = ing Kemp’s ridley sea turtles nesting season: onset vs. end (p =
0.0275; and C) end, p = 0.0456. Different letters indicate signifi- 0.0206571), middle vs. end (p = 0.0327514). Different letters in-
cant differences. dicate significant differences.
148Rapid stress response in post-nesting Lepidochelys kempii
to acute stress because they have fewer relative energy re- male Kemp’s ridley sea turtles respond quickly to a stressor
serves compared to larger species (Wingfield et al. 1995); stimulus, and at the end of the nesting season they man-
this could explain the rapid response to stress, generating a age to reduce the concentration of CORT with respect to
high concentration of CORT. the beginning of the season, so the modulation of the HPA
The stress response recorded in L. kempii was faster than axis helps them to successfully conclude all nesting events
other species of sea turtles. For example, suppression of during the season.
hormonal response has been recorded for nesting females
of C. mydas and E. imbricata suppression, as they do not
show high CORT levels after capture (Jessop 2001), in con- Acknowledgements
trast to the significant increase found in Kemp’s ridley nest- We thank Miriam Barradas and Genaro Coria for assistance
ing females. A stress modulation response has been ob- with laboratory analysis. We thank Emilio Suárez Domínguez
served in species such as Lepidochelys olivacea (Valverde and Ibiza Martínez Serrano for valuable comments to manu-
et al. 1999) and Dermochelys coriacea (Rostal et al. 2001, script. We thank Centro Tortuguero Santander and CICE for lo-
Al-Habsi et al. 2006), and the modulation of the HPA axis gistical support. We thank Denise Spaan for their comments and
allow them to maximize reproductive investment (Jessop english support on this manuscript. Our research was support-
2001). However, our results suggest that this characteris- ed by The Consejo Nacional de Ciencia y Tecnología of Mexico
tic is not shared by L. kempi, which has a lower sensitiv- (CONACyT) through a graduate scholarship to OSVB (Scholar-
ship #337177).
ity threshold to stressors than other sea turtles because it
shows rapid activation in the HPA axis. This strategy may
aid survival, improving their ability to stay alert, as being a
uniquely diurnal nesting species they are exposed to great- References
er risk factors during the nesting season.
Aguirre, A. A., G. H. Balazs, T. R. Spraker & T. S. Gross (1995):
In nesting Kemp’s ridley sea turtles CORT levels de- Adrenal and hematological responses to stress in juvenile green
creased between 0.78 and 7.1 times to the end compared to turtles (Chelonia mydas) with and without fibropapillomas. –
the beginning of the stress protocol. Immature individu- Physiological Zoology, 68: 831–854.
als CORT concentration increase 7.2-fold after 30-min. re- Al-Habsi, A. A., A. Y. A. Alkindi, I. Y. Mahmoud, D. W. Owens,
tention (Gregory et al. 1996), and they increased 15 times T. Khan & A. al-Abri (2006): Plasma hormone levels in the
in the face of acute stress during net capture (Gregory & green turtles Chelonia mydas during peak period of nesting at
Schmid 2001). In both afore mentioned studies, CORT’s Ras Al-Hadd-Oman. – Journal of endocrinology, 191: 9–14.
levels increase in the stress test’s final was greater than our Bolton, M. (2008): Energy e, body-weight and foraging perform-
investigation. Those results were consistent with other sea ance of Storm Petrels Hydrobates pelagicus breeding in artificial
turtle species where immature individuals show higher nesting chambers. – Ibis, 138: 405–409.
HPA axis activation than nesting females (Aguirre et al. Bonnet, X., G. Naulleau & R. Mauget (1994): The influence of
1995, Valverde et al. 1999, Moore & Jessop 2003, Hunt body condition on 17-b estradiol levels in relation to vitellogen-
et al. 2012). We recorded differences in CORT levels at the esis in female Vipera aspis. – General and Comparative Endo-
beginning, middle, and end of the nesting season. We ex- crinology, 93: 424–437.
pected an increase in CORT levels as the nesting season Caillouet, C. W. Jr (2014): Interruption of the Kemp’s ridley
progressed due to the possible loss of energy reserves and population’s pre-2010 exponential growth in the Gulf of Mexi-
deterioration of the female’s body condition during the pe- co and its aftermath: one hypothesis. – Marine Turtle Newslet-
ter, 143: 1–7.
riod of aphagia; however, contrary to expectation, we ob-
served a significant decrease in CORT concentration at Cherel, Y., J. P. Robin & Y. L. Maho (1988): Physiology and bio-
the end of the nesting season. Similarly, Whittier et al. chemistry of long-term fasting in birds. – Canadian Journal of
Zoology, 66: 159–166.
(1997) found CORT concentrations of Caretta caretta (Lin-
naeus, 1758) to decrease significantly during the nesting Cherel, Y., R. Mauget, A. Lacroix & J. Gilles (1994): Seasonal
and fasting-related changes in circulating gonadal steroids and
season, suggesting that basal CORT level stabilize, as has prolactin in king penguins, Aptenodytes patagonicus. – Physio
been observed in immature individuals. Nesting female logical Zoology, 67: 1154–1173.
C. mydas did not reach critical body condition levels af-
Crain, A. & L. J. Guillette Jr (2000): Environmental endocrine
ter the nesting season, suggesting that the body does not disruptors: an evolutionary perspective. – CRC Press, Wash-
perceive prolonged periods of aphagia as a stressor (Ha- ington DC.
mann et al. 2002). Sea turtles display seasonal physiologi- Derickson, W. K. (1976): Lipid storage and utilization in reptiles.
cal changes that function to regulate annual reproductive – American Zoologist, 16: 711–723.
patterns, and at the end of the nesting season, body dete- Gregory, L. F., T. S. Gross, A. B. Bolten, K. A. Bjorndal & L. J.
rioration can be minimized, allowing the females to reach Guillette Jr (1996): Plasma corticosterone concentrations as-
the feeding sites (Rostal et al. 1998). The variation in cor- sociated with acute captivity stress in wild loggerhead sea tur-
ticosterone concentration in our study and other species of tles (Caretta caretta). – General and comparative endocrinol-
marine turtles demonstrates the need for further studies ogy, 104: 312–320.
that take environmental conditions and the individuals’ in- Gregory, L. F. & J. R. Schmid (2001): Stress responses and sexing
trinsic conditions into account. In conclusion, nesting fe- of wild Kemp’s ridley sea turtles (Lepidochelys kempii) in the
149Ozzy S. Vásquez Bultrón et al.
northeastern Gulf of Mexico. – General and comparative en- Donnelly (eds): Técnicas de investigación y manejo para la
docrinology, 124: 66–74. conservación de las tortugas marinas. Grupo Especialista en
Hamann, M., C. Limpus & J. Whittier (2002): Patterns of lipid Tortugas Marinas UICN/CSE Publicación Nº 4. – Consolidat-
storage and mobilization in the female green sea turtle (Chelo- ed Graphic Communications, Blanchard, Pennsylvania, USA.
nia mydas). – Journal of Comparative Physiology B, 172: 485– R Core Team (2013): R: A language and environment for statistical
493. computing. R Foundation for Statistical Computing, – R Core
Hamann, M. C. J., C. Limpus & D. W. Owens (2003): Reproduc- Team, Vienna, Austria.
tive cycles of males and females. – pp. 135–161 in: Lutz, P. L., J. Rostal, D. C., T. R. Robeck, J. S. Grumbles & P. M. Burchfield
A. Musick & J. Wyneken (eds): The biology of sea turtle: vol. (1998): Seasonal reproductive cycle of the Galapagos tortoise
II. – CRC Press, Washington DC. (Geochelone nigra) in captivity. – Zoo Biology, 17: 505–517.
Hays, G. C., A. C. Broderick, F. Glen & B. J. Godley (2002): Rostal, D. C., J. S. Grumbles, K. S. Palmer, V. A. Lance, J. R.
Change in body mass associated with long-term fasting in a Spotila & F. V. Paladino (2001): Changes in gonadal and ad-
marine reptile: the case of green turtles (Chelonia mydas) at As- renal steroid levels in the leatherback sea turtle (Dermochelys
cension Island. – Canadian Journal of Zoology, 80: 1299–1302. coriacea) during the nesting cycle. – General and Comparative
Hunt, K. E., C. Innis & R. M. Rolland (2012): Corticoster- Endocrinology, 122: 139–147.
one and thyroxine in cold-stunned Kemp’s ridley sea turtles Santos, A. J., E. M. Freire, C. Bellini & G. Corso (2010):
(Lepidochelys kempii). – Journal of Zoo and Wildlife Medicine, Body mass and the energy budget of gravid hawksbill turtles
43: 479–493. (Eretmochelys imbricata) during the nesting season. – Journal
Hunt, K. E., C. J. Innis, A. E. Kennedy, K. L. McNally, D. G. of Herpetology, 44: 352–360.
Davis, E. A. Burgess & C. Merigo (2016): Assessment of Spotila, J. R. & E. A. Standora (1985): Environmental con-
ground transportation stress in juvenile Kemp’s ridley sea tur- straints on the thermal energetics of sea turtles. – Copeia, 1985:
tles (Lepidochelys kempii). – Conservation physiology, 4: 1–13. 694–702.
Islam, M. S. & M. Tanaka (2004): Impacts of pollution on coastal Stephenson, K., P. Vargas & D. W. Owens (2000): Diurnal cy-
and marine ecosystems including coastal and marine fisheries cling of corticosterone in a captive population of Kemp’s rid-
and approach for management: a review and synthesis. – Ma- ley sea turtles (Lepidochelys kempii) – pp. 232–233 in: Abreu-
rine Pollution Bulletin, 48: 624–649. Grobois, F. A., R. Briseño-Dueñas, R. Márquez & L. Sarti
Jessop, T. S. (2001): Modulation of the adrenocortical stress re- (compilers): Proceeding of the Eighteenth International Sym-
sponse in marine turtles (Cheloniidae): evidence for a hor- posium. – U.S. Department of Commerce, National Oceanic
monal tactic maximizing maternal reproductive investment. – and Atmospheric Administration, National Marine Fisheries
Journal of Zoology, 254: 57–65. Service, Southeast Fisheries Science Center, Miami, USA.
Jessop, T. S., J. M. Sumner, C. J. Limpus & J. M. Whittier (2004): Valverde, R. A. (1996): Corticosteroid dynamics in a free-rang-
Interplay between plasma hormone profiles, sex and body ing population of olive ridley sea turtles (Lepidochelys olivacea
condition in immature hawksbill turtles (Eretmochelys imbri- Eschscholtz, 1829) at playa Nancite, Costa Rica as a function
cata) subjected to a capture stress protocol. – Comparative of their reproductive behavior. – Doctoral thesis, Texas A&M
Biochemistry and Physiology Part A: Molecular & Integrative University, Austin, Texas, USA.
Physiology, 137: 197–204. Valverde, R. A., D. W. Owens, D. S. Mackenzie & M. S. Amoss
Lewison, R. L., L. B. Crowder & D. J. Shaver (2003): The impact (1999): Basal and stress-induced corticosterone levels in olive
of turtle excluder devices and fisheries closures on loggerhead ridley sea turtles (Lepidochelys olivacea) in relation to their
and Kemp’s ridley strandings in the western Gulf of Mexico. – mass nesting behavior. – Journal of Experimental Zoology,
Conservation Biology, 17: 1089–1097. 284: 652–662.
Lewison, R. L., S. A. Freeman & L. B. Crowder (2004): Quanti- Wallace, B. P., R. L. Lewison, S. L. McDonald, R. K. McDon-
fying the effects of fisheries on threatened species: the impact ald, C. Y. Kot, S. Kelez, R. K. Bjorkland, E. M. Finkbeiner,
of pelagic longlines on loggerhead and leatherback sea turtles. S. Helmbrecht & L. B. Crowder (2010): Global patterns of
– Ecology Letters, 7: 221–231. marine turtle bycatch. – Conservation Letters, 3: 131–142.
Madsen, T. & R. Shine (2000): Energy versus risk: costs of repro- Whittier, J. M., F. Corrie & C. Limpus (1997): Plasma ster-
duction in free-ranging pythons in tropical Australia. – Austral oid profiles in nesting loggerhead turtles (Caretta caretta) in
Ecology, 25: 670–675. Queensland, Australia: relationship to nesting episode and
season. – General and Comparative Endocrinology, 106: 39–
Márquez, R. (1996): Las tortugas marinas y nuestro tiempo. – 47.
Impresora y Encuadernadora Progreso, México.
Williams, C. T., A. S. Kitaysky, A. B. Kettle & C. L. Buck
Moore, I. T. & T. S. Jessop (2003): Stress, reproduction, and (2008): Corticosterone levels of tufted puffins vary with breed-
adrenocortical modulation in amphibians and reptiles. – Hor- ing stage, body condition index, and reproductive perform-
mones and Behavior, 43: 39–47. ance. – General and Comparative Endocrinology, 158: 29–35.
Norris, D. O. & J. A. Carr (2013): Vertebrate endocrinology. Aca- Wingfield, J. C., K. M. O’Reilly & L. B. Astheimer (1995): Mod-
demic Press, USA. ulation of the adrenocortical responses to acute stress in arc-
Owens, D. W. & G. J. Ruiz (1980): New methods of obtaining tic birds: a possible ecological basis. – American Zoologist, 35:
blood and cerebrospinal fluid from marine turtles. – Herpeto- 285–294.
logica, 36: 17–20. Wingfield, J. C., D. L. Maney, C. W. Breuner, J. D. Jacobs, S.
Pritchard, P. C. H. & J. A. Mortimer (2000): Taxonomía, mor- Lynn, M. Ramenofsky & R. D. Richardson (1998): Ecologi-
fología externa e identificación de las especies. – pp. 23–41 in: cal bases of hormone – behavior interactions: the “emergency
Eckert, K. L., K. A. Bjorndal, F. A. Abreu-Grobois & M. life history stage”. – American Zoologist, 38: 191–206.
150You can also read
